OPEN spawning in the Gulf of Oman and

SUBJECT AREAS: relationship to latitudinal variation in COMMUNITY ECOLOGY ECOSYSTEM ECOLOGY spawning season in the northwest Indian

Received Ocean 8 September 2014 E. J. Howells1, D. Abrego2, G. O. Vaughan1 & J. A. Burt1 Accepted 26 November 2014 1Center for Genomics and Systems Biology, New York University Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates, Published 2Department of Natural Science and Public Health, Zayed University, PO Box 144534, Abu Dhabi, United Arab Emirates. 15 December 2014

Despite a wealth of information on sexual reproduction in scleractinian , there are regional gaps in reproductive records. In the Gulf of the Oman in the Arabian Sea, reproductive timing was assessed Correspondence and in four common species of broadcast spawning corals using field surveys of gamete maturity and requests for materials aquarium observations of spawning activity. The appearance of mature gametes within the same month should be addressed to for downingi, A. hemprichii, Cyphastrea microphthalma and Platygyra daedalea ($ 75% of E.J.H. (em.howells@ colonies, n 5 848) indicated a synchronous and multi-specific spawning season. Based on gamete gmail.com) disappearance and direct observations, spawning predominantly occurred during April in 2013 (75– 100% of colonies) and May in 2014 (77–94% of colonies). The difference in spawning months between survey years was most likely explained by sea temperature and the timing of lunar cycles during late-stage gametogenesis. These reproductive records are consistent with a latitudinal gradient in peak broadcast spawning activity at reefs in the northwestern Indian Ocean which occurs early in the year at low latitudes (January to March) and progressively later in the year at mid (March to May) and high (June to September) latitudes.

exual reproduction in scleractinian corals can occur in a variety of forms but the majority of species (.60%) are simultaneous hermaphrodites that spawn both eggs and sperm into the water column1,2. Broadcast spawning allows cross-fertilization between individuals and development of planktonic larvae allows new S 3,4 coral genotypes to disperse across short and large distances . Recruitment of coral larvae is critical to the persistence and recovery of coral assemblages5,6 and enhances adaptive potential by increasing local genetic variation7–9. Broadcast spawning in most individual corals occurs during one or a few nights per year following an annual cycle of gametogenesis2. Synchronous spawning within populations enhances their reproductive success and proposed environmental cues including sea temperature and lunar phase promote spawning during discrete seasons and nights10. Numerous studies of coral reproductive patterns demonstrate coral spawning around the warmest months of the year, yet the duration of spawning seasons and the extent of synchronicity among species and individuals can vary considerably among locations (see reviews by1,2,9,11). Consequently, localised investi- gations are required to determine precise spawning months and nights in data deficient regions. The aim of our study was to record spawning behaviour in corals from the Gulf of Oman, Arabian Sea, for which there were no previous records. We investigated the seasonal and lunar timing of spawning for 4 locally abundant scleractinian species using a combination of 2 years of field surveys and aquarium observa- tions. Locally, these data provide important baseline information for monitoring the health of coral com- munities in the Gulf of Oman which are periodically impacted by damage from fishing gear and anchors12, cyclones13, outbreaks of predatory crown-of-thorns starfish12, oil pollution14,15 and harmful algal blooms16. More broadly, these data contribute to a growing number of records of coral spawning activity in the northwest Indian Ocean17–22 which allowed us to examine latitudinal patterns in spawning behaviour and their underlying environmental drivers.

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(a) 54°E 56°E 58°E 60°E 62°E (b)

I r a n (c) 26°N A r a b i a n / P e r s i a n

Survey site G u l f s (d) e t a G u l f o f O m a n r i m E 24°N

a b A r O U n i t e d m a n A r a b i a n (e)

S e a 100 km

Figure 1 | Location of reproductive surveys in the Gulf of Oman (a) for the scleractinian corals Acropora downingi (b), Acropora hemprichii (c), Cyphastrea microphthalma (d), Platygyra daedalea (e). Map created by using Adobe Illustrator CS5.

Results the lunar cycle or around the new moon. Between 10 nights after the Sexual reproduction was seasonally synchronous in the scleractinian April full moon and 4 nights before the May full moon in 2014, the corals Acropora downingi, A. hemprichii, Cyphastrea microphthalma percentage of colonies with mature gametes sharply declined from and Platygyra daedalea common to the Gulf of Oman23 (Fig. 1). 81% (n 5 53) to 5% (n 5 58) in A. downingi and from 95% (n 5 41) Mature gametes developed in $ 75% of colonies of each species prior to 33% in A. hemprichii. This reproductive timing is supported by to one of the spring full-moons and disappeared by the following aquarium spawning of A. downingi (n 5 8) which occurred in all month, indicating that spawning had occurred (Fig. 2a). In 2013, the colony fragments on 13 and/or 14 nights after the full moon (i.e. new majority of colonies belonging to each species (75 to 100%) moon) in April 2013. developed mature gametes by the April full moon (25th), whereas in 2014, gamete maturation did not occur in most colonies (77 to Discussion th 94%) until prior to the May full moon (14 ). This inter-annual Patterns of sexual reproduction in corals from the Gulf of Oman variation in spawning timing corresponded with lower monthly demonstrate that coral communities in the northern Arabian Sea average sea temperatures in the lead up to the 2014 spawning, includ- engage in seasonally synchronous spawning events, such as those ing average sea temperature preceding the April full moon that were that have been observed in numerous other tropical and temperate 1.5uC lower in 2014 compared with 2013 (Fig. 2b). reef ecosystems (e.g. refs. 10, 25, 26). The April to May timing of Additional field and aquarium observations of Gulf of Oman cor- spawning in acroprid and merulind corals observed in the Gulf of als demonstrated variation in the lunar phase of spawning among the Oman is consistent with spawning months of corals from these fam- 24 coral species being studied. The merulinids (formerly favids ) C. ilies at latitudes (22–27uN) from nearby regions of the Arabian/ microphthalma and P. daedalea spawned around the full moon, as Persian Gulf17 and the Red Sea20,27. At lower latitude (13uN) in the indicated by the timing of disappearance of mature eggs between 4 southern Arabian Sea, surveys of egg maturity indicate that at least days before and 12 days after the full moon in May 2014 (Table 1). half of the acroporid corals spawn in February and March22 which is The percentage of colonies with mature eggs declined from 88% (n 5 consistent with the peak of spawning activity in acroporid and mer- 25) to 23% (n 5 21) in C. microphthalma and from 56% (n 5 41) to ulinid corals from equatorial reefs in the Indian Ocean18,19. In con- 0% (n 5 42) in P. daedalea. A small proportion (22%) of P. daedalea trast, at higher latitude (30uN), broadcast spawning in most coral colonies had mature gamete bundles 7 days before the full moon in species occurs from June to September (northern Red Sea28). These April. These colonies likely began spawning after the April full moon results combined show a latitudinal gradient in seasonality of peak and may have still been releasing by the next survey 10 days after the broadcast spawning activity in corals from the northwest Indian full moon. Thus, the high proportion of colonies found with mature Ocean with spawning earlier in the year close to the equator and bundles 10 days after the April full moon may reflect colonies that later in the year with increasing northward latitude (r50.75, p were still spawning as well as those colonies with bundles mature ,0.01, Fig. 3). enough to be released after the May full moon. This interpretation is Coral spawning during annual periods of sea temperature rise has supported by an extended spawning window observed in fragments been well documented29. Latitudinal differences in spawning seasons from individual P. daedalea colonies (n 5 10) kept in aquaria in April in the northwest Indian Ocean are likely due to variation in temper- 2013. These colonies released gametes for up to 10 consecutive ature profiles and are consistent with latitudinal trends in coral nights. Spawning occurred from 19:45 to 21:30 (1:00 to 2:45 hours reproduction in the northwest Pacific30. For example, sites closer to after sunset) from 2 nights before the full moon to 9 nights after the the equator (,13uN; sites 10, 12–13 in Fig. 3) reach their annual full moon (when observations ceased), with a spawning peak 3 nights maximum temperatures earlier in the year (March to May) com- after full moon when all colony fragments released gametes. pared with higher latitude sites (.22uN; sites 5–9 in Fig. 3) which In contrast, field surveys of the acroporids A. downingi and A. reach their maximum later in the year (July to August). The delayed hemprichii indicated that the majority of colonies spawned later in spawning peak at the highest latitude and coolest region of the Red

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(a) (i) Acropora downingi (ii) Acropora hemprichii

4 45 6 41 100 40 35 100 40 Immature 53 80 80 4 Mature 60 60 40 40

20 20

Individuals (%) Individuals Individuals (%) Individuals 58 40 0 50 * 0 * * * 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 March April May June March April May June

(iii) Cyphastrea microphthalma (iv) Platygyra daedalea 20 14 100 14 33 100 30 80 80 60 60 40 40 21 50

20 20

Individuals (%) Individuals Individuals (%) Individuals 50 50 42 0 * * * * 0 * * 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 2013 2014 March April May June March April May June

(b)

31 2013 30 2014 29 28 27 26 25 24 23 22

Lunar cycle average temperature (°C) temperature average cycle Lunar 21 January February March April May June 27th /16th 25th /14th 27th /16th 25th /15th 25th /14th 23rd /13th Date of full moon in 2013 / 2014 Figure 2 | Percentage of coral colonies in the Gulf of Oman with visibly immature and mature eggs (a) and sea temperatures (b) during 2013 and 2014. Coral species surveyed were Acropora downingi (i), Acropora hemprichii (ii), Cyphastrea microphthalma (iii), Platygyra daedalea (iv). Note that for (iv), immature eggs could not be distinguished from an absence of eggs. Sample sizes are provided in italicized text above columns and asterisks indicate months when no surveys were undertaken. Sea temperatures are the monthly average preceding each full moon during the coral spawning season in 2013 and 2014 in the Gulf of Oman. Monthly minimum and maximum values and annual trends are provided in the Electronic Supplementary Material.

Table 1 | Field (a) and aquarium (b) observations of the lunar phase of spawning in the Gulf of Oman. Sample sizes are provided in italicized text in parentheses

(a) Colonies with mature gametes in the field on nights relative to full moon in 2014 (b) Aquarium spawning on nights Coral species 27 April 110 April 24 May 112 May relative to full moon in April 2013 Acropora downingi 9% (45) 81% (53) 5% (58) - 113 to 114 (10) Acropora hemprichii 3% (40) 95% (41) 33% (42) 0% (40) - Cyphastrea microphthalma - 77% (30) 88% (25) 23% (21) - Platygyra daedalea 22% (50) 94% (33) 56% (41) 0% (42) 22to19 (peak 13) (8)

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30°N 1 2 A ra b ia n 4 3 5 G A s i a ulf 6 7 9 8 A r a b i a n R 20°N e P e n i n s u l a d S e a 10 A r a b i a n S e a

A f r i c a 11 12 10°N

Month J F M A M J J A S I n d i a n O c e a n 13

0° 500 km 14 40°E 50°E 60°E 70°E

Figure 3 | Latitudinal trends in peak broadcast spawning activity in corals from the northwest Indian Ocean. Peak activity from January (J) to September (S) was classed as the month(s) when the majority of individuals and species were directly observed or inferred (from spawn slicks or assays of gamete maturity) to have spawned. 1: Eilat28, 2: Kuwait42, 3: Hurghada20, 4: Kish and Larak (pers. comm M. Shokri, M. Moradi), 5: Tarout37, 6: Fujairah (this study), 7: Dubai17, 8: Gujarat43, 9: Thuwal21, 10: Farasan44, 11: Socotra22, 12: Lakshadweep (pers. comm S. Subburaman), 13: Maldives45, 14: Mombassa18,19. The correlation co-efficient between site latitude and spawning month, r, is 0.75 (p ,0.01). Map created by using Adobe Illustrator CS5.

Sea (sites 1–2, 4 in Fig 3) may reflect a lag in reaching temperatures A. downingi spawning around the new moon and A. hemprichii that are optimal for reproduction (i.e. cross-fertilization and embryo- possibly also spawning at this time. Consequently, further observa- genesis31,32). In the Gulf of Oman, variation in the predominant tions are required to confirm the lunar phase of spawning in acro- spawning month between survey years is likely due to entrainment porids from the Gulf of Oman. of spawning activity to the optimal temperature window1. When the The data presented provide the first records of sexual reproduction full moon falls early in the month29,33 and/or if the onset of seasonal in corals from the Gulf of Oman. Broadcast spawning in four com- warming is delayed, gamete maturation and spawning (in all or some mon species of scleractinian corals occurs during the same month(s) corals in the population) is often delayed until the consecutive lunar of April to May but is spread across different phases of the lunar cycle29,33,34. Additionally, corals that have been moved to warmer or cycle. While the timing of coral spawning in the Gulf of Oman is cooler environments during their gametogenic cycle often have seasonally consistent with regions of the Indian Ocean at similar accelerated or delayed spawning35,36 further supporting temperature latitude, further work is required to investigate the extent of repro- as a strong driver of spawning month. ductive synchrony among additional coral species and localities in Species-specific variation in the lunar phase of spawning in the the Gulf of Oman and the wider Arabian Sea. Gulf of Oman corresponded to the spawning nights previously reported for the investigated merulinid species but was relatively Methods unusual for the acroporid species. Spawning of Cyphastrea micro- Reproductive behaviour was surveyed in A. downingi, A. hemprichii, Cyphastrea phthalma and Platygyra daedalea within 5 days of the full moon has microphthalma and Platygyra daedalea in the Gulf of Oman (Fig. 1). The survey 17 area was located on shallow inshore reefs (, 6m depth) spanning a 15 km been observed in the nearby Arabian Gulf as well as distant Indo- stretch of the coastline of Fujairah in the United Arab Emirates. Specifically, Pacific localities10,29. However, the observation that individual P. surveys were conducted at 25u36911.840N/56u2192.700E, 25u29932.740N/ daedalea colonies from the Gulf of Oman release gametes for up to 56u21948.920Eand25u28956.610N/56u21956.140E. To determine the lunar 10 consecutive nights suggests an extended spawning period for this cycle(s) during which coral species were spawning, surveys were conducted in the week prior to each full moon from March to June in 2013 and 2014 during species compared to other localities (ref. 10, personal observations), the transition between winter and summer as spawning typically occurs during a although we cannot exclude the possibility that spawning behaviour period of sea temperature rise or fall29,39. Within the survey area, average sea was altered by aquarium conditions. Earlier records of spawning in temperatures across each lunar cycle were calculated from 30-minute readings A. downingi (Red Sea21, Arabian Gulf37 (as A. clathrata, see ref. 38)) from a temperature logger (HOBOH pendant, OnsetH)attachedtothereef 21 substrate at Al Aqah reef. and A. hemprichii (Red Sea ) document gamete release within 4 A total of 848 colonies (.20 cm diameter) were haphazardly surveyed across the nights of the full moon. This is in contrast to our observations of duration of the study and the sample sizes for each of four species and eight survey

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months are provided in Fig. 2. Reproductive timing was inferred from the appearance 22. Baird, A., Abrego, D., Howells, E. & Cumbo, V. The reproductive season of and disappearance of mature eggs within the population following the methodology Acropora in Socotra, Yemen. F1000Research 3 (2014). and categories of Baird et al.40. Coral colonies with pigmented eggs were scored as 23. Claereboudt, M. Reef corals and coral reefs of the Gulf of Oman. (Historical reproductively mature and likely to spawn during the current or following lunar cycle. Association of Oman, 2006). Corals with very pale or white eggs were scored as reproductively immature and likely 24. Huang, D. et al. Taxonomic classification of the reef coral families Merulinidae, to spawn during the following 1–2 lunar cycles. Corals with no visible eggs were either Montastraeidae, and Diploastraeidae (: : ). Zool. J. very immature and unlikely to spawn during the next 2 lunar cycles, had recently Linn. Soc. 171, 277–355 (2014). spawned, or did not reproduce during the survey year. In A. downingi and A. hem- 25. Szmant, A. Reproductive ecology of Caribbean reef corals. Coral reefs 5, 43–53 prichii, egg maturity was assessed by removing one branch from the center of each (1986). colony for in situ examination of gametes at the branch base well below their expected 26. Babcock, R., Wills, B. & Simpson, C. Mass spawning of corals on a high latitude sterile zone41. In instances where no eggs were observed, two additional branches were coral reef. Coral Reefs 13, 161–169 (1994). sampled to confirm that the coral colony did not contain any visible eggs. In C. 27. Bouwmeester, J., Khalil, M., De La Torre, P. & Berumen, M. Synchronous microphthalma and P. daedalea, egg pigmentation was assessed by removing 3 cm2 spawning of Acropora in the Red Sea. Coral Reefs 30, 1011–1011 (2011). sections of coral tissue from the center of each colony with a hammer and chisel. C. 28. Shlesinger, Y. & Loya, Y. Coral community reproductive patterns: red sea versus microphthalma samples were examined ex situ under a microscope and P. daedalea the great barrier reef. Science 228, 1333–1335 (1985). samples were examined in situ using a magnifying glass. In P. daedalea, we were 29. Willis, B., Babcock, R., Harrison, P. & Oliver, J. Patterns in the mass spawning of unable to distinguish between immature eggs and the absence of eggs. corals on the Great Barrier Reef from 1981 to 1984. Proc. Int. Symp. Coral Reefs, To identify the lunar phase (or nights) during which coral species were spawning, a 5th 4, 343–348 (1985). combination of field and laboratory observations were undertaken. During the month 30. Harii, S., Omori, M., Yamakawa, H. & Koike, Y. Sexual reproduction and larval when the proportion of pigmented eggs were highest in 2014, an additional field settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes. survey of gamete maturation was conducted in the week prior to the new moon to Coral Reefs 20, 19–23 (2001). determine whether eggs where disappearing (i.e. being spawned) around the new or 31. Keshavmurthy, S., Fontana, S., Mezaki, T., del Can˜o Gonza´lez, L. & Chen, C. full phases of the moon. Additionally, fragments from 8 colonies of A. downingi and Doors are closing on early development in corals facing climate change. Sci. Rep. 4 10 colonies of P. daedalea containing pigmented eggs were collected one week before (2014). the April full moon in 2013 and observed nightly for spawning activity (gamete 32. Woolsey, E., Byrne, M. & Baird, A. The effects of temperature on embryonic ‘‘setting’’ and/or release). Fragments were maintained in recirculating aquaria at New development and larval survival in two scleractinian corals. Mar. Ecol. Prog. Ser. York University Abu Dhabi with daylight illumination and isolation in darkness at 493, 179–184 (2013). sunset each evening. 33. Hayashibara, T. et al. Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar. Ecol. Prog. Ser. 101, 263–272 (1993). 34. Nozawa, Y. Annual variation in the timing of coral spawning in a high-latitude 1. Baird, A., Guest, J. & Willis, B. Systematic and Biogeographical Patterns in the environment: influence of temperature. Biol. Bull. 222, 192–202 (2012). Reproductive Biology of Scleractinian Corals. Annu. Rev. Ecol. Syst. 40, 551–571 35. Fan, T.-Y. & Dai, C.-F. Reproductive plasticity in the reef coral Echinopora (2009). lamellosa. Mar. Ecol. Prog. Ser. 190, 297–301 (1999). 2. Harrison, P. & Wallace, C. Reproduction, dispersal and recruitment of 36. Howells, E., Berkelmans, R., van Oppen, M., Willis, B. & Bay, L. Historical thermal scleractinian corals. Ecosyst. World 25, 133–207 (1990). regimes define limits to coral acclimatization. Ecology 94, 1078–1088 (2013). 3. Jones, G. et al. Larval retention and connectivity among populations of corals and 37. Fadlallah, Y. Synchronous spawning of Acropora clathrata coral colonies from the reef fishes: history, advances and challenges. Coral Reefs 28, 307–325 (2009). western Arabian Gulf (Saudi Arabia). Bull. Mar. Sci. 59, 209–216 (1996). 4. Graham, E., Baird, A. & Connolly, S. Survival dynamics of scleractinian coral 38. Wallace, C. Staghorn corals of the world: a revision of the coral genus Acropora larvae and implications for dispersal. Coral reefs 27, 529–539 (2008). (Scleractinia; Astrocoeniina; ) worldwide, with emphasis on 5. Gilmour, J., Smith, L., Heyward, A., Baird, A. & Pratchett, M. Recovery of an morphology, phylogeny and biogeography. (CSIRO publishing, 1999). isolated coral reef system following severe disturbance. Science 340, 69–71 (2013). 39. Simpson, C. Mass spawning of scleractinian corals in the Dampier Archipelago 6. Colgan, M. Coral reef recovery on Guam (Micronesia) after catastrophic and the implications for management of coral reefs in Western Australia. predation by Acanthaster planci. Ecology 68, 1592–1605 (1987). Department of Conservation and Environment Perth, Bulletin 244, 1–35 (1985). 7. van Oppen, M. & Gates, R. Conservation genetics and the resilience of reef- 40. Baird, A., Marshall, P. & Wolstenholme, J. Latitudinal variation in the building corals. Mol. Ecol. 15, 3863–3883 (2006). reproduction of Acropora in the Coral Sea. Proc. Int. Symp. Coral Reefs, 9th 1, 8. van Oppen, M. Souter, P., Howells, E., Heyward, A. & Berkelmans, R. Novel 385–389 (2002). genetic diversity through somatic mutations: fuel for adaptation of reef corals? 41. Soong, K. & Lang, J. Reproductive integration in reef corals. Biol. Bull. 183, Diversity 3, 405–423 (2011). 418–431 (1992). 9. Richmond, R. [Reproduction and recruitment in corals: Critical links in the 42. Carpenter, K., Harrison, P., Hodgson, G., Alsaffar, A. & Alhazeem, S. The corals persistence of reefs] Life and death of coral reefs [Birkeland, C. (ed.)] [175–197] and coral reef fishes of Kuwait (Kuwait Institute for Scientific Research, Kuwait, (Chapman & Hall, New York, 1997). 1997). 10. Babcock, R. et al. Synchronous spawnings of 105 scleractinian coral species on the 43. Subburaman, S., Gouthan, S., Adhavan, D. & Jothi, P. Preliminary observation of Great Barrier Reef, Australia. Mar. Biol. 90, 379–394 (1986). Mass Coral Spawning slicks at Mithapur reef,Gulf of Kachchh, West Coast of 11. Harrison, P. [Sexual Reproduction of Scleractinian Corals] Coral reefs: an India. Asian J. Mar. Sci. 1, 31–33 (2013). ecosystem in transition [Dubinsky, Z., Stambler N. (eds.)] [59–85] (Springer, 44. Gladstone, W. Unique annual aggregation of longnose parrotfish (Hipposcarus Heidelberg, 2011). harid) at Farasan Island (Saudi Arabia, Red Sea). Copeia 1996, 483–485 (1996). 12. Salm, R. Coral Reefs of the Sultanate of Oman. Atoll Res. Bull. 380, 1–83 (1993). 45. Sier, C. & Olive, P. Reproduction and reproductive variability in the coral 13. Foster, K., Foster, G., Tourenq, C. & Shuriqi, M. Shifts in coral community Pocillopora verrucosa from the Republic of Maldives. Mar. Biol. 118, 713–722 structures following cyclone and red tide disturbances within the Gulf of Oman (1994). (United Arab Emirates). Mar. Biol. 158, 955–968 (2011). 14. Shriadah, M. Impacts of an oil spill on the marine environment of the United Arab Emirates along the Gulf of Oman. Mar. Pollut. Bull. 36, 876–879 (1998). 15. El Samra, M. & El Deeb, K. Horizontal and vertical distribution of oil pollution in Acknowledgments the Arabian Gulf and the Gulf of Oman. Mar. Pollut. Bull. 19, 14–18 (1988). This study was permitted by the Fujairah Municipality and Dibba Municipality and 16. Bauman, A., Burt, J., Feary, D., Marquis, E. & Usseglio, P. Tropical harmful algal logistical support was provided by the Palms Dive Center. Research funding was provided blooms: An emerging threat to coral reef communities? Mar. Pollut. Bull. 60, by New York University, Zayed University, the Mohammed bin Zayed Species 2117–2122 (2010). Conservation Fund, and the Ford Motor Company Conservation and Environment Fund. 17. Bauman, A., Baird, A. & Cavalcante, G. Coral reproduction in the world’s warmest reefs: southern Persian Gulf (Dubai, United Arab Emirates). Coral Reefs 30, 405–413 (2011). Author contributions 18. Mangubhai, S. & Harrison, P. Gametogenesis, spawning and fecundity of E.J.H. designed the study. E.J.H., D.A. and G.O.V. collected data. E.J.H. wrote the Platygyra daedalea (Scleractinia) on equatorial reefs in Kenya. Coral Reefs 27, manuscript with contribution from D.A. and J.A.B. 117–122 (2008). 19. Mangubhai, S. & Harrison, P. Extended breeding seasons and asynchronous Additional information spawning among equatorial reef corals in Kenya. Mar. Ecol. Prog. Ser. 374, Supplementary information accompanies this paper at http://www.nature.com/ 305–310 (2009). scientificreports 20. Hanafy, M., Aamer, M., Habib, M., Rouphael, A. & Baird, A. Synchronous reproduction of corals in the Red Sea. Coral Reefs 29, 119–124 (2010). Competing financial interests: The authors declare no competing financial interests. 21. Bouwmeester, J. et al. Multi-species spawning synchrony within scleractinian How to cite this article: Howells, E.J., Abrego, D., Vaughan, G.O. & Burt, J.A. Coral coral assemblages in the Red Sea. Coral Reefs, 1–13. DOI:10.1007/s00338-014- spawning in the Gulf of Oman and relationship to latitudinal variation in spawning season 1214-6. in the northwest Indian Ocean. Sci. Rep. 4, 7484; DOI:10.1038/srep07484 (2014).

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